Carhart-Harris’s Entropic Brain Hypothesis

Psychopharmacologist Robin Carhart-Harris proposes the Entropic Brain Hypothesis in which the entropy of spontaneous brain activity indexes the informational richness of conscious states (within upper and lower limits, after which consciousness may be lost). A leading psychedelic researcher, Carhart-Harris reports that the entropy of brain activity is elevated in the psychedelic state, and there is evidence for greater brain “criticality” under psychedelics. (“Criticality … is the property of being poised at a ‘critical’ point in a transition zone between order and disorder where certain phenomena such as power-law scaling appear.”) He argues that “heightened brain criticality enables the brain to be more sensitive to intrinsic and extrinsic perturbations which may translate as a heightened susceptibility to ‘set’ and ‘setting.’” Measures of brain entropy, he suggests, can inform the treatment of psychiatric and neurological conditions such as depression and disorders of consciousness (Carhart-Harris, 2018).

Entropy, Criticality, and Primary States

The “entropy” in the Entropic Brain Hypothesis is defined as “a dimensionless quantity that is used for measuring uncertainty about the state of a system but it can also imply physical qualities, where high entropy is synonymous with high disorder.” Entropy is then applied in “the context of states of consciousness and their associated neurodynamics, with a particular focus on the psychedelic state … [which] is considered an exemplar of a primitive or primary state of consciousness that preceded the development of modern, adult, human, normal waking consciousness.”

Based on neuroimaging data with psilocybin, a classic psychedelic drug, Carhart-Harris argues that “the defining feature of ‘primary states’ is elevated entropy in certain aspects of brain function, such as the repertoire of functional connectivity motifs that form and fragment across time. Indeed, since there is a greater repertoire of connectivity motifs in the psychedelic state than in normal waking consciousness, this implies that primary states may exhibit ‘criticality’” (Carhart-Harris, 2018).

Significantly, “if primary states are critical, then this suggests that entropy is suppressed in normal waking consciousness, meaning that the brain operates just below criticality.” This leads to the idea that “entropy suppression furnishes normal waking consciousness with a constrained quality and associated metacognitive functions, including reality-testing and self-awareness.” Carhart-Harris and colleagues also propose that “entry into primary states depends on a collapse of the normally highly organized activity within the default-mode network” (DMN—a set of regions more active during passive tasks than tasks requiring focused external attention, Buckner, 2013),^[1] thus maintaining the brain's homeostasis and “a decoupling between the DMN and the medial temporal lobes (which are normally significantly coupled)” (Carhart-Harris et al., 2014).

Neural Signatures and Broader Applications

Increased entropy in spontaneous neural activity is one of the most notable neurophysiological signatures of psychedelics and is said to be relevant to the psychedelic experience, mediating both acute alterations in consciousness and long-term effects. While overall entropy increases, entropy changes are not uniform across the brain: entropy increases in all regions, but the larger effect is localized in visuooccipital regions. At the whole-brain level, this reconfiguration is related closely to the topological properties of the brain's anatomical connectivity (Herzog et al., 2023).

(For how psychedelic experiences and mechanisms may or may not inform theories of consciousness, see Psychedelic Theories of Consciousness.)

Computational neuroscientist Gustavo Deco uses the concept of equilibrium in physics to explore consciousness. Since a physical system is in equilibrium when in its most stable state, the question is how close to equilibrium are the electrical states of the brain while people perform different tasks? Using a sophisticated mathematical theorem to analyze neuroimaging data, “they found that the brain is closer to a state of equilibrium when people are gambling than when they are cooperating,” suggesting that “there are many shades of consciousness” (Callaghan, 2024).

Footnote

[1]. It is also active during directed tasks that require participants to remember past events or imagine upcoming events (Buckner, 2013).